Characterization of extended-spectrum cephalosporins and fluoroquinolone resistance of a Salmonella enterica serovar Thompson isolate from ready-to-eat pork product in China

Salmonella is a leading cause of foodborne illness worldwide and is a common concern in food safety. Salmonella enterica displaying resistance to extended-spectrum cephalosporins (ESCs) and fluoroquinolone (FQs) has been deemed a high-priority pathogen by the World Health Organization. Co-resistance to ESCs and FQs has been reported in S. enterica serovar Thompson (S. Thompson). However, the genetic context of ESCs and FQs resistance genes in S. Thompson lacks sufficient characterization. In this study, we characterized a multi-drug resistant (MDR) S. Thompson isolate recovered from a retail ready-to-eat (RTE) pork product in China. Short- and long-read sequencing (HiSeq and MinION) of the genome identified the presence of bla(CMY-2), qnrS1, and qepA8, along with 11 additional acquired antimicrobial resistance genes, residing on a 152,940 bp IncA/C plasmid. Specifically, the bla(CMY-2), qnrS1, and qepA8 genes were located in insertion sequences (ISs) and integron mediated mobile genetic structure, sugE-blc-bla(CMY-2)-ISEc9, IS26-orf6-qnrS1-orf5-ISKpn19, and intl1-qepA8-orf10-IS91-orf1-dfrA12-orf11-aadA2-qacE Delta 1-sul1, respectively. Each gene was identified in various bacteria species, indicating their high transfer ability. The plasmid was found to be transferable to Escherichia coli J53 by conjugation and resulted in the acquiring of multiple resistances in the transconjugants. The plasmid is closely related to plasmids from two human S. Thompson strains isolated in different regions and years in China. Moreover, core-genome Multi Locus Sequence Typing (cgMLST) and phylogenetic analysis based on global 1,868 S. Saintpaul isolates showed that the S. Thompson isolate was highly epidemiologically linked to a human isolate in China. Our findings suggest that Chinese RTE pork products are a possible source of human pathogenic ESCs and FQs co-resistant S. Thompson. Furthermore, the results underline the important role of conjugative plasmids in acquiring and transmission of ESCs and FQs resistance in S. Thompson isolates, which need continuous investigation.

Automated summary

This study characterized a multi-drug resistant Salmonella Thompson isolate from retail ready-to-eat pork products in China and identified resistance genes located on a plasmid with high transferability. The plasmid is closely related to human Salmonella Thompson strains in China. The findings suggest that Chinese RTE pork products may be a possible source of pathogenic Salmonella Thompson with co-resistance to ESCs and FQs.